Pseudomonas aeruginosa flagellar motility activates the phagocyte PI3K/Akt pathway to induce phagocytic engulfment

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 306, Issue 7, 2014, Pages

  Lovewell, Rustin R ^a   Hayes, Sandra M ^b   O'Toole, George A ^a   Berwin, Brent ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Akt; Flagellar motility; Phagocytosis; Pseudomonas aeruginosa

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE LYN;

ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; BACTERIAL CLEARANCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLAGELLUM; HUMAN; HUMAN CELL; LUNG ALVEOLUS MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

AKT; FLAGELLAR MOTILITY; PHAGOCYTOSIS; PSEUDOMONAS AERUGINOSA;

ACTINS; ANIMALS; FLAGELLA; MACROPHAGES, ALVEOLAR; MICE; PHAGOCYTOSIS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION;

EID: 84900524942     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00319.2013     Document Type: Article

References (36)

1. Amiel E, Lovewell RR, O'Toole GA, Hogan DA, Berwin B. Pseudomonas aeruginosa evasion of phagocytosis is mediated by loss of swimming motility and is independent of flagellum expression. Infect Immun 78: 2937-2945, 2010.
2. Balloy V, Verma A, Kuravi S, Si-Tahar M, Chignard M, Ramphal R. The role of flagellin versus motility in acute lung disease caused by Pseudomonas aeruginosa. J Infect Dis 196: 289-296, 2007.
3. Braun TF, Poulson S, Gully JB, Empey JC, Van Way S, Putnam A, Blair DF. Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J Bacteriol 181: 3542-3551, 1999.
4. Choi YJ, Im E, Chung HK, Pothoulakis C, Rhee SH. TRIF mediates Toll-like receptor 5-induced signaling in intestinal epithelial cells. J Biol Chem 285: 37570-37578, 2010.
5. Doyle TB, Hawkins AC, McCarter LL. The complex flagellar torque generator of Pseudomonas aeruginosa. J Bacteriol 186: 6341-6350, 2004.
6. Duncan MJ, Li G, Shin JS, Carson JL, Abraham SN. Bacterial penetration of bladder epithelium through lipid rafts. J Biol Chem 279: 18944-18951, 2004.
7. Feldman M, Bryan R, Rajan S, Scheffler L, Brunnert S, Tang H, Prince A. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect Immun 66: 43-51, 1998.
8. Finger EB, Puri KD, Alon R, Lawrence MB, von Andrian UH, Springer TA. Adhesion through L-selectin requires a threshold hydrodynamic shear. Nature 379: 266-269, 1996.
9. Flannagan RS, Jaumouille V, Grinstein S. The cell biology of phagocytosis. Annu Rev Pathol 7: 61-98, 2012.
10. Folkesson A, Jelsbak L, Yang L, Johansen HK, Ciofu O, Hoiby N, Molin S. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nat Rev Microbiol 10: 841-851, 2012.
11. Freter R, O'Brien PC, Macsai MS. Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect Immun 34: 234-240, 1981.
12. Hannigan MO, Huang CK, Wu DQ. Roles of PI3K in neutrophil function. Curr Top Microbiol Immunol 282: 165-175, 2004.
13. Inaba K, Inaba M, Deguchi M, Hagi K, Yasumizu R, Ikehara S, Muramatsu S, Steinman RM. Granulocytes, macrophages, and dendritic cells arise from a common major histocompatibility complex class IInegative progenitor in mouse bone marrow. Proc Natl Acad Sci USA 90: 3038-3042, 1993.
14. Kannan S, Audet A, Huang H, Chen LJ, Wu M. Cholesterol-rich membrane rafts and Lyn are involved in phagocytosis during Pseudomonas aeruginosa infection. J Immunol 180: 2396-2408, 2008.
15. Kierbel A, Gassama-Diagne A, Mostov K, Engel JN. The phosphoinositol-3-kinase-protein kinase B/Akt pathway is critical for Pseudomonas aeruginosa strain PAK internalization. Mol Biol Cell 16: 2577-2585, 2005.
16. Kierbel A, Gassama-Diagne A, Rocha C, Radoshevich L, Olson J, Mostov K, Engel J. Pseudomonas aeruginosa exploits a PIP3-dependent pathway to transform apical into basolateral membrane. J Cell Biol 177: 21-27, 2007.
17. Koh AY, Priebe GP, Ray C, Van Rooijen N, Pier GB. Inescapable need for neutrophils as mediators of cellular innate immunity to acute Pseudomonas aeruginosa pneumonia. Infect Immun 77: 5300-5310, 2009.
18. Lane MC, Lockatell V, Monterosso G, Lamphier D, Weinert J, Hebel JR, Johnson DE, Mobley HL. Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 73: 7644-7656, 2005.
19. Lovewell RR, Collins RM, Acker JL, O'Toole GA, Wargo MJ, Berwin B. Step-wise loss of bacterial flagellar torsion confers progressive phagocytic evasion. PLoS Pathog 7: e1002253, 2011.
20. Luzar MA, Thomassen MJ, Montie TC. Flagella and motility alterations in Pseudomonas aeruginosa strains from patients with cystic fibrosis: relationship to patient clinical condition. Infect Immun 50: 577-582, 1985.
21. Lyczak JB, Cannon CL, Pier GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060, 2000.
22. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15: 194-222, 2002.
23. Mahenthiralingam E, Campbell ME, Speert DP. Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun 62: 596-605, 1994.
24. Mahenthiralingam E, Speert DP. Nonopsonic phagocytosis of Pseudomonas aeruginosa by macrophages and polymorphonuclear leukocytes requires the presence of the bacterial flagellum. Infect Immun 63: 4519-4523, 1995.
25. Mijares LA, Wangdi T, Sokol C, Homer R, Medzhitov R, Kazmierczak BI. Airway epithelial MyD88 restores control of Pseudomonas aeruginosa murine infection via an IL-1-dependent pathway. J Immunol 186: 7080-7088, 2011.
26. Murray TS, Egan M, Kazmierczak BI. Pseudomonas aeruginosa chronic colonization in cystic fibrosis patients. Curr Opin Pediatr 19: 83-88, 2007.
27. Olsen JE, Hoegh-Andersen KH, Casadesus J, Rosenkranzt J, Chadfield MS, Thomsen LE. The role of flagella and chemotaxis genes in host pathogen interaction of the host adapted Salmonella enterica serovar Dublin compared with the broad host range serovar S. typhimurium. BMC Microbiol 13: 67, 2013.
28. Patankar YR, Lovewell RR, Poynter ME, Jyot J, Kazmierczak BI, Berwin B. Flagellar motility is a key determinant of the magnitude of the inflammasome response to Pseudomonas aeruginosa. Infect Immun 81: 2043-2052, 2013.
29. Rhee SH, Kim H, Moyer MP, Pothoulakis C. Role of MyD88 in phosphatidylinositol 3-kinase activation by flagellin/toll-like receptor 5 engagement in colonic epithelial cells. J Biol Chem 281: 18560-18568, 2006.
30. Ruby EG, Asato LM. Growth and flagellation of Vibrio fischeri during initiation of the sepiolid squid light organ symbiosis. Arch Microbiol 159: 160-167, 1993.
31. Shiratsuchi H, Basson MD. Akt2, but not Akt1 or Akt3 mediates pressure-stimulated serum-opsonized latex bead phagocytosis through activating mTOR and p70 S6 kinase. J Cell Biochem 102: 353-367, 2007.
32. Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, Duronio V, Finlay BB. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 275: 37718-37724, 2000.
33. Toutain CM, Zegans ME, O'Toole GA. Evidence for two flagellar stators and their role in the motility of Pseudomonas aeruginosa. J Bacteriol 187: 771-777, 2005.
34. Triantafilou M, Brandenburg K, Kusumoto S, Fukase K, Mackie A, Seydel U, Triantafilou K. Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem J 381: 527-536, 2004.
35. Weichhart T, Saemann MD. The PI3K/Akt/mTOR pathway in innate immune cells: emerging therapeutic applications. Ann Rheum Dis 67, Suppl 3: iii70-iii74, 2008.
36. Weiner OD, Neilsen PO, Prestwich GD, Kirschner MW, Cantley LC, Bourne HR. A PtdInsP(3)-and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity. Nat Cell Biol 4: 509-513, 2002.